Characterization and in vitro culture of male germ cells from developing bovine testis

Journal of Reproduction and Development

Volumn 57, Issue 3, 2011, Pages 355-364

  Fujihara, Mayako ^a   Kim, Sung Min ^a   Minami, Naojiro ^a   Yamada, Masayasu ^a   Imai, Hiroshi ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Gonocytes; Spermatogenesis; Spermatogonia; Stem cells; Testis

Indexed keywords

BIOLOGICAL MARKER; HOMEODOMAIN PROTEIN; OCTAMER TRANSCRIPTION FACTOR; UBIQUITIN THIOLESTERASE;

ANIMAL; ARTICLE; CATTLE; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MOUSE; MOUSE MUTANT; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; TESTIS;

ANIMALS; BIOLOGICAL MARKERS; CATTLE; CELL PROLIFERATION; CELLS, CULTURED; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, SCID; OCTAMER TRANSCRIPTION FACTORS; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS; TESTIS; UBIQUITIN THIOLESTERASE;

ANIMALIA; BOVINAE; DOLICHOS; DOLICHOS BIFLORUS; MUS;

EID: 79960126108     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.10-185M     Document Type: Article

References (52)

1. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957; 100: 241-267.
2. McLean DJ, Friel PJ, Johnston DS, Griswold MD. Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice. Biol Reprod 2003; 69: 2085-2091.
3. Aponte PM, de Rooij DG, Bastidas P. Testicular development in Brahman bulls. Theriogenology 2005; 64: 1440-1455.
4. Amann RP. Endocrine changes associated with onset of spermatogenesis in Holstein bulls. J Dairy Sci 1983; 66: 2606-2622.
5. Curtis SK, Amann RP. Testicular development and establishment of spermatogenesis in Holstein bulls. J Anim Sci 1981; 53: 1645-1657.
6. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 2000; 93: 139-149.
7. Tanaka SS, Toyooka Y, Akasu R, Katoh Fukui Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 2000; 14: 841-853.
8. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci USA 1994; 91: 11298-11302.
9. Pesce M, Wang X, Wolgemuth DJ, Scholer H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. Mech Dev 1998; 71: 89-98.
10. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 2003; 69: 612-616.
11. Kanatsu-Shinohara M, Kato M, Takehashi M, Morimoto H, Takashima S, Chuma S, Nakatsuji N, Hirabayashi M, Shinohara T. Production of transgenic rats via lentiviral transduction and xenogeneic transplantation of spermatogonial stem cells. Biol Reprod 2008; 79: 1121-1128.
12. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. Transgenic mice produced by retroviral transduction of male germ line stem cells in vivo. Biol Reprod 2004; 71: 1202-1207.
13. Nagano M, Brinster CJ, Orwig KE, Ryu BY, Avarbock MR, Brinster RL. Transgenic mice produced by retroviral transduction of male germ-line stem cells. Proc Natl Acad Sci USA 2001; 98: 13090-13095.
14. Hamra FK, Gatlin J, Chapman KM, Grellhesl DM, Garcia JV, Hammer RE, Garbers DL. Production of transgenic rats by lentiviral transduction of male germ-line stem cells. Proc Natl Acad Sci USA 2002; 99: 14931-14936.
15. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. Genetic selection of mouse male germline stem cells in vitro: offspring from single stem cells. Biol Reprod 2005; 72: 236-240.
16. Kanatsu-Shinohara M, Muneto T, Lee J, Takenaka M, Chuma S, Nakatsuji N, Horiuchi T, Shinohara T. Long-term culture of male germline stem cells from hamster testes. Biol Reprod 2008; 78: 611-617.
17. Kanatsu-Shinohara M, Inoue K, Lee J, Yoshimoto M, Ogonuki N, Miki H, Baba S, Kato T, Kazuki Y, Toyokuni S, Toyoshima M, Niwa O, Oshimura M, Heike T, Nakahata T, Ishino F, Ogura A, Shinohara T. Generation of pluripotent stem cells from neonatal mouse testis. Cell 2004; 119: 1001-1012.
18. Seandel M, James D, Shmelkov SV, Falciatori I, Kim J, Chavala S, Scherr DS, Zhang F, Torres R, Gale NW, Yancopoulos GD, Murphy A, Valenzuela DM, Hobbs RM, Pandolfi PP, Rafii S. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 2007; 449: 346-350.
19. Conrad S, Renninger M, Hennenlotter J, Wiesner T, Just L, Bonin M, Aicher W, Buhring HJ, Mattheus U, Mack A, Wagner HJ, Minger S, Matzkies M, Reppel M, Hescheler J, Sievert KD, Stenzl A, Skutella T. Generation of pluripotent stem cells from adult human testis. Nature 2008; 456: 344-349.
20. Izadyar F, Den Ouden K, Creemers LB, Posthuma G, Parvinen M, De Rooij DG. Proliferation and differentiation of bovine type A spermatogonia during long-term culture. Biol Reprod 2003; 68: 272-281.
21. Oatley JM, Reeves JJ, McLean DJ. Biological activity of cryopreserved bovine spermatogonial stem cells during in vitro culture. Biol Reprod 2004; 71: 942-947.
22. Aponte PM, Soda T, van de Kant HJ, de Rooij DG. Basic features of bovine spermatogonial culture and effects of glial cell line-derived neurotrophic factor. Theriogenology 2006; 65: 1828-1847.
23. Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJ, de Rooij DG. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 2008; 136: 543-557.
24. Dobrinski I, Avarbock MR, Brinster RL. Germ cell transplantation from large domestic animals into mouse testes. Mol Reprod Dev 2000; 57: 270-279.
25. Ertl C, Wrobel KH. Distribution of sugar residues in the bovine testis during postnatal ontogenesis demonstrated with lectin-horseradish peroxidase conjugates. Histochemistry 1992; 97: 161-171.
26. Wrobel KH, Bickel D, Kujat R, Schimmel M. Configuration and distribution of bovine spermatogonia. Cell Tissue Res 1995; 279: 277-289.
27. Wrobel KH. Prespermatogenesis and spermatogoniogenesis in the bovine testis. Anat Embryol (Berl) 2000; 202: 209-222.
28. Bartholomew RA, Parks JE. Identification, localization, and sequencing of fetal bovine VASA homolog. Anim Reprod Sci 2007; 101: 241-251.
29. Fujihara M, Goel S, Minami N, Yamada M, Imai H. Cryopreservation in liquid nitrogen of gonocytes from neonatal porcine testes stored at 4°C. Reprod Med Biol 2008; 7: 153-160.
30. Herrid M, Davey RJ, Hill JR. Characterization of germ cells from pre-pubertal bull calves in preparation for germ cell transplantation. Cell Tissue Res 2007; 330: 321-329.
31. Izadyar F, Spierenberg GT, Creemers LB, den Ouden K, de Rooij DG. Isolation and purification of type A spermatogonia from the bovine testis. Reproduction 2002; 129: 85-94.
32. Ji M, Minami N, Yamada M, Imai H. Effect of protopanaxatriol saponin on spermatogenic stem cell survival in busulfan-treated male mice. Reprod Med Bio 2007; 6: 99-108.
33. Goel S, Fujihara M, Minami N, Yamada M, Imai H. Expression of NANOG, but not POU5F1, points to the stem cell potential of primitive germ cells in neonatal pig testis. Reproduction 2008; 135: 785-795.
34. Devkota B, Sasaki M, Takahashi K, Matsuzaki S, Matsui M, Haneda S, Takahashi M, Osawa T, Miyake Y. Postnatal developmental changes in immunohistochemical localization of alpha-smooth muscle actin (SMA) and vimentin in bovine testes. J Reprod Dev 2006; 52: 43-49.
35. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 2000; 97: 9585-9590.
36. Lee GS, Kim HS, Lee SH, Kang MS, Kim DY, Lee CK, Kang SK, Lee BC, Hwang WS. Characterization of pig vasa homolog gene and specific expression in germ cell lineage. Mol Reprod Dev 2005; 72: 320-328.
37. Mitchell RT, Cowan G, Morris KD, Anderson RA, Fraser HM, Mckenzie KJ, Wallace WH, Kelnar CJ, Saunders PT, Sharpe RM. Germ cell differentiation in the marmoset (Callithrix jacchus) during fetal and neonatal life closely parallels that in the human. Hum Reprod 2008; 23: 2755-2765.
38. Hoei-Hansen CE, Almstrup K, Nielsen JE, Brask Sonne S, Graem N, Skakkebaek NE, Leffers H, Rajpert De Meyts E. Stem cell pluripotency factor NANOG is expressed in human fetal gonocytes, testicular carcinoma in situ and germ cell tumours. Histopathology 2005; 47: 48-56.
39. Lee J, Kim HK, Rho JY, Han YM, Kim J. The human OCT-4 isoforms differ in their ability to confer self-renewal. J Biol Chem 2006; 281: 33554-33565.
40. Atlasi Y, Mowla SJ, Ziaee SA, Gokhale PJ, Andrews PW. OCT4 spliced variants are differentially expressed in human pluripotent and nonpluripotent cells. Stem Cells 2008; 26: 3068-3074.
41. Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, Tongaonkar HB. Newer insights into pre-meiotic development of germ cells in adult human testis using Oct-4 as a stem cell marker. J Histochem Cytochem 2010; 58: 1093-1106.
42. Looijenga LH, Stoop H, de Leeuw HP, de Gouveia Brazao CA, Gillis AJ, van Roozendaal KE, van Zoelen EJ, Weber RF, Wolffenbuttel KP, van Dekken H, Honecker F, Bokemeyer C, Perlman EJ, Schneider DT, Kononen J, Sauter G, Oosterhuis JW. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res 2003; 63: 2244-2250.
43. Kuijk EW, de Gier J, Lopes SM, Chambers I, van Pelt AM, Colenbrander B, Roelen BA. A distinct expression pattern in mammalian testes indicates a conserved role for NANOG in spermatogenesis. PLoS One 2010; 5: e10987.
44. Maki CB, Pacchiarotti J, Ramos T, Pascual M, Pham J, Kinjo J, Anorve S, Izadyar F. Phenotypic and molecular characterization of spermatogonial stem cells in adult primate testes. Hum Reprod 2009; 24: 1480-1491.
45. Luo J, Megee S, Dobrinski I. Asymmetric distribution of UCH-L1 in spermatogonia is associated with maintenance and differentiation of spermatogonial stem cells. J Cell Physiol 2009; 220: 460-468.
46. Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Yoshida S, Toyokuni S, Lee J, Ogura A, Shinohara T. Leukemia inhibitory factor enhances formation of germ cell colonies in neonatal mouse testis culture. Biol Reprod 2007; 76: 55-62.
47. Chen C, Ouyang W, Grigura V, Zhou Q, Carnes K, Lim H, Zhao GQ, Arber S, Kurpios N, Murphy TL, Cheng AM, Hassell JA, Chandrashekar V, Hofmann MC, Hess RA, Murphy KM. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436: 1030-1034.
48. Kubota H, Avarbock MR, Brinster RL. Culture conditions and single growth factors affect fate determination of mouse spermatogonial stem cells. Biol Reprod 2004; 71: 722-731.
49. Ryu BY, Kubota H, Avarbock MR, Brinster RL. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci USA 2005; 102: 14302-14307.
50. Ogawa T, Ohmura M, Tamura Y, Kita K, Ohbo K, Suda T, Kubota Y. Derivation and morphological characterization of mouse spermatogonial stem cell lines. Arch Histol Cytol 2004; 67: 297-306.
51. Ko K, Tapia N, Wu G, Kim JB, Bravo MJ, Sasse P, Glaser T, Ruau D, Han DW, Greber B, Hausdorfer K, Sebastiano V, Stehling M, Fleischmann BK, Brustle O, Zenke M, Scholer HR. Induction of pluripotency in adult unipotent germline stem cells. Cell Stem Cell 2009; 5: 87-96.
52. Sadri-Ardekani H, Mizrak SC, van Daalen SK, Korver CM, Roepers-Gajadien HL, Koruji M, Hovingh S, de Reijke TM, de la Rosette JJ, van der Veen F, de Rooij DG, Repping S, van Pelt AM. Propagation of human spermatogonial stem cells in vitro. JAMA 2009; 302: 2127-2134.